Anales del Jardín Botánico de Madrid 77 (2): e099 https://doi.org/10.3989/ajbm.2558 ISSN-L: 0211-1322

Rediscovery of the endangered lichen Pseudocyphellaria aurata (Lobariaceae, Ascomycota) in mainland Spain

Ibai OLARIAGA1, Graciela PAZ-BERMÚDEZ2, Javier CALVO3, Javier ETAYO4, María PRIETO5* 1,5 Department of Biology and Geology, Physics and Inorganic Chemistry, Rey Juan Carlos University, Calle Tulipán s.n., 28933 Móstoles, Madrid, Spain. 2,3 Universidade de Vigo, Escola de Enxeñaría Forestal, Departamento ERNMA, A Xunqueira s.n., 36005 Pontevedra, Spain. 4 Navarro Villoslada 16, 3º dcha., E-31003 Pamplona, Navarra, Spain.

*Correspondence: [email protected] 1https://orcid.org/0000-0002-0334-7750, 2https://orcid.org/0000-0003-3724-8483, 3https://orcid.org/0000-0002-1732-9449, 4https://orcid.org/0000-0003-0392-0710, 5https://orcid.org/0000-0002-1692-9821

Abstract. Lichens, as well as other organisms, should be considered Resumen. Los líquenes son una parte importante de la biodiversidad que important biodiversity components for the establishment of priorities in debería tenerse en cuenta para establecer prioridades en la biología de la conservation biology. In this study, we report six new recent localities of conservación. En este estudio, se citan 6 nuevas localidades en las que el the highly endangered, epiphytic macrolichen Pseudocyphellaria aurata in líquen epífito Pseudocyphellaria aurata, gravemente amenazado, ha sido Spain: two in Navarra and four in A Coruña. Previous Spanish reports based hallado recientemente: 2 localidades en Navarra y 4 en A Coruña. Registros on literature and herbarium specimens suggest a reduction of the distribution bibliográficos y especímenes de herbario previos sugieren que P. aurata ha area of P. aurata and local extinction. Pseudocyphellaria aurata is known to sufrido una regresión en su área de distribución. Se considera P. aurata extinta en be extinct in six localities, where it has not been observed since the middle 6 localidades en las que no se ha observado desde mediados del siglo XIX (Cádiz, of the 19th century (Cádiz, Pontevedra, Málaga). Four records reported for Pontevedra, Málaga). Cuatro citas del centro peninsular (Zaragoza, Salamanca, central Spain (Zaragoza, Salamanca, Teruel) are considered unplausible. Teruel) no se consideran plausibles. Todas las nuevas localidades albergan The newly discovered populations are located in well-preserved patches of manchas bien conservadas de bosque atlántico, en lugares con fuerte influencia atlantic deciduous forest with strong oceanic influence, whose long-term oceánica y con presencia de árboles centenarios que sugieren continuidad ecological stability seems evident because of the presence of ancient trees. ecológica. Sin embargo, las poblaciones de P. aurata descubiertas son pequeñas, Nevertheless, these populations are small, fragmentary, and are threatened by fragmentadas, y están amenazadas por degradación de hábitat, explotación habitat degradation, forestry and maybe fungal pathogens. Two populations, forestal y quizás, hongos patógenos. Dos poblaciones, Intzola y Beba (Navarra Intzola and Beba (Navarra and A Coruña, respectively), account for 75.7% of y A Coruña, respectivamente), albergan el 75,7 % de los talos. Las localidades thalli. The localities with the highest number of trees colonized by P. aurata en las que se han contabilizado más árboles colonizados por P. aurata son Santa are Santa Leocadia and Beba in A Coruña. We reassessed the conservation Leocadia y Beba en A Coruña. Con los datos recopilados, evaluamos el estado de status of this species concluding that conservation initiatives must be conservación de P. aurata, concluyendo que deben de implementarse iniciativas implemented to avoid its extinction in mainland Spain. de conservación para evitar su extinción en la España peninsular.

Keywords. Conservation biology, IUCN, local extinction, red-listing. Palabras clave. Biología de la conservación, extinción local, IUCN, listas rojas.

How to cite this article: Olariaga I., Paz-Bermúdez G., Calvo J., Etayo J., Prieto M. 2020. Rediscovery of the endangered lichen Pseudocyphellaria aurata (Lobariaceae, Ascomycota) in mainland Spain. Anales del Jardín Botánico de Madrid 77: e099. https://doi.org/10.3989/ajbm.2558 Title in Spanish: Redescubrimiento del líquen amenazado Pseudocyphellaria aurata (Lobariaceae, Ascomycota) en la España peninsular. Associate Editor: Isabel Martínez. Received: 18 April 2020; accepted: 7 October 2020; published online: 4 January 2021.

INTRODUCTION The family Lobariaceae includes foliose macrolichens mostly associated with well-preserved forest ecosystems. The Although numerous threats are currently affecting global whole family, although not yet formally listed in the IUCN Red biodiversity, lichens are often overlooked when establishing List, has been proposed for Global Red Listing because the priorities for conservation biology (IUCN 2015). Given the majority of its species are probably threatened (Baillie & al. importance of epiphytic lichens in many forest ecosystems 2004). Pseudocyphellaria aurata (Ach.) Vain. is probably one (Hayward & Rosentreter 1994), and their value as indicators of the most threatened species of Lobariaceae in continental of environmental changes and climatic conditions (Benítez Europe and has been included in a number of national and & al. 2012; Matos & al. 2015), these organisms should be regional red lists (e.g., Woods & Coppins 2012; Kon & Ohmura considered in conservation initiatives. In order to evaluate the 2014; Roux & al. 2016). With a cosmopolitan distribution in conservation status of lichen species, a deep understanding of tropical areas of the world (Galloway 1998), P. aurata is also the ecology and distribution of the target species is required found in drier, warmer, coastal areas in cool temperate regions (Scheidegger & Werth 2009).

Copyright: © 2020 CSIC. This is an open-access article distributed under the Creative Commons Attribution-Non Commercial Lisence (CC BY 4.0). Olariaga & al. 2

(Galloway & Arvidsson 1990). In Europe, P. aurata is a rare of Lobariaceae (Moncada & al. 2013) does not resolve the species reported from Great Britain, France, Italy, Portugal, and relationships among lineages assigned to Pseudocyphellaria Spain (Degelius 1935; Nimis & Martellos 2017), whereas the s.l., so far a morphologically well recognizable genus. Thus, records from Switzerland are considered doubtful (Nimis 1993). we consider it premature to split Pseudocyphellaria into European populations of P. aurata have been stated to be in several smaller genera. This avoids unnecessary changes if the decline in France (Roux & al. 2016) and Great Britain (Smith & monophyly of Pseudocyphellaria s.l. is demonstrated by future al. 2009), and to be extinct in Italy (Nimis & Martellos 2017), phylogenetic analyses. but the general state of the populations remains unknown in Coordinates are provided in decimal format (WGS84). Europe (Serusiaux 1989) including the Iberian Peninsula. For each new species occurrences, the exact locality, In their revision of Iberian Lobariaceae, Burgaz & Martínez approximate elevation above sea level, annual precipitation (1999) cited material from 10 localities in Portugal, but one and temperature were recorded. Climatic data were obtained single from Spain (Carballal & al. 1985), collected in 1978 from Meteogalicia (www.meteogalicia.gal/observacion/rede/ (SANT-Lich. 133) in Fragas do Eume Natural Park (A Coruña). redeIndex.action?request_locale=gl) and Meteorología y Despite visiting this locality several times, P. aurata has not Climatología de Navarra (http://meteo.navarra.es/estaciones/ been found there again (López de Silanes, pers. comm). mapadeestaciones.cfm) webpages. Annual mean temperature The presence of Pseudocyphellaria aurata in mainland and annual precipitation were calculated based on all Spain prior to the report by Carballal & al. (1985) is enigmatic. available data from the nearest station to each site and located Although quite a few reports exist, no specimens or recent at a similar altitude. Herbarium specimens were examined observations have been made since the 19th century and it either by loaning herbarium specimens (H-Ach), during is unclear whether bibliographic reports of P. aurata can be visits to herbaria (PC, I. Olariaga) or by viewing high-quality attributed to misidentifications. Pseudocyphellaria aurata scans (MAF-Lich, PC) when available. Material from Bertiz has been reported from Andalusia (Colmeiro 1867; Jovet (Navarra) and Intzola populations (Navarra) of P. aurata is 1941) and the French Basque Country (Jovet 1941). During deposited in ARAN-Fungi fungarium (Thiers 2020). his doctoral thesis, Etayo (1989) searched for P. aurata, intensively in Navarra without success, and that led Etayo (2002) to consider it extinct in the Western Pyrenees. However, RESULTS more recent finds in southern France (Vivant 1988) and in the Pseudocyphellaria aurata has been found in six new Pyrénées Atlantiques department (Roux & al. 2016), not far localities in Spain, two in Navarra (Bertiz, Intzola) and from the boundary with Spain, support the possibility that four in A Coruña (Albariña, Beba, Devesa de Anllares, P. aurata is present in the Spanish Pyrenees. Santa Leocadia), and was also re-discovered in the French During fieldwork in the Western Pyrenees and Galicia, Pyrenean locality (Intzola, French Basque Country) cited by Pseudocyphellaria aurata was found in six new localities and Jovet (1941). However, P. aurata was searched for without was also rediscovered in the same locality from which Jovet success in Canuto del Risco Blanco (Los Barrios, Cádiz), La (1941) reported it more than 80 years ago, 500 m from the Sauceda (Cortes de la Frontera, Málaga), Inpernuko erreka Spanish border. Since P. aurata is a threatened species for (Etxalar, Navarra), Endarlatsa erreka (Lesaka-Irun, Navarra- which very little updated information exists, the main goal of Gipuzkoa), Altzolarats erreka (Aia-Zestoa, Gipuzkoa) and this study was to compile all the information available about many other valleys from Navarra and Basque Country. A list its presence in mainland Spain. These data are of paramount of the new populations of P. aurata, with detailed descriptions importance to assess the conservation status of P. aurata of the sites, number of trees colonized, number of thalli, under the IUCN criteria, not only in Spain, but also in Europe, accompanying species and conservation threats, is provided and indispensable for its inclusion in conservation initiatives. below. In addition, a list of previous localities reported in the literature or supported by herbarium specimens is given.

MATERIAL AND METHODS New localities Pseudocyphellaria aurata was searched for in lowland A summary of the newly discovered localities, with oceanic localities with well-preserved deciduous forests with the number of thalli and trees colonized by P. aurata ancient trees, in A Coruña, Biscay, Cádiz, Gipuzkoa, Málaga and phorophytes, is provided in Table 1. Localities are and Navarra. The number of thalli and trees colonized by represented on a map (Fig. 1). Populations in which more P. aurata were counted at each locality. Accompanying species thalli were counted are Intzola and Beba, with 97 and 60 were identified following Smith & al. (2009) for lichenized thalli respectively, which account for 73% of thalli found fungi and Casas & al. (2006, 2009) for mosses and liverworts. in this study. Populations with the highest numbers of Nomenclature follows Index Fungorum as a rule. Exceptions colonized trees were Santa Leocadia and Beba, with 10 and are Arthonia pelvetii (Linds.) H. Olivier (placement in 9, respectively. In Intzola, the population with the highest Homostegia Fuckel not accepted, a genus with perithecioid number of thalli, P. aurata was found only on three trees. ascomata) and P. aurata (placecement in Crocodia Link not Although P. aurata was found on several, mostly acid-barked, accepted). As for the latter, the latest phylogenetic hypothesis tree species, Castanea sativa Mill. and Quercus robur L. were

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Table 1. Newly found populations and subpopulations of the epiphytic macrolichen Pseudocyphellaria aurata in Spain. Coordinates, number of thalli, trees colonized, height at which thalli grew, and phorophytes are provided.

Trees Height Province Pop. Subp. Coord. Thalli Col. Orient. (m) Phorophyte Navarra Bertiz Ber1 43.172982 -1.604253 2 1 N 1.5 Salix atrocinerea Ber2 43.161839 -1.611640 4 2 - 6–8 Alnus glutinosa Subtotal 6 3 Navarra/ Pyrenées Intzola Int1 43.318772 -1.673708 10, 23 2 N 1–3 Quercus robur Atlantiques Int2 43.306154 -1.669580 64 1 W 1.5–3 Platanus hispanica Subtotal 97 3 A Coruña La Devesa de An1 42.946339 -9.079122 31 7 S–SW 1–1.6 Quercus robur Anllares Subtotal 31 7 A Coruña Albariña Alb 42.928357 -8.740161 1 1 S 1.9 Castanea sativa Subtotal 1 1 Beba Beba Beb1 42.902208 -9.012094 1, 4 2 SW 1.5–1.7 Quercus robur Beb2 42.895278 -9.011078 20, 10, 3 3 SW 0.4–1.6 Castanea sativa, Sambucus nigra Beb3 42.893803 -9.011258 1, 1, 17 3 SW 0.6–1.7 Castanea sativa Beb4 42.892014 -9.010208 11 1 SW 0.7–1.7 Castanea sativa Subtotal 68 8 A Coruña Santa SL1 42.899644 -8.922139 1, 1, 1, 1, 2, 2 6 SW 0.7–1.3 Corylus avellana, Laurus nobilis Leocadia SL2 42.899869 -8.922097 2, 2 2 SW 0.9–1.2 Quercus robur, Corylus avellana SL3 42.897581 -8.924231 4, 3 2 SW 1.7–2.3 Quercus robur Subtotal 19 10 Total 222 32

the most common phorophytes (Table 1) on which P. aurata subpopulations were found at this locality (Table 1): Beba 1, colonizes mostly mossy bark in rather sun-exposed situations. with one and four thalli in two Quercus robur trees together Remarkably, P. aurata was also found on an allochthonous with Parmeliella triptophylla. Lobarina scrobiculata, planted Platanus hispanica Mill. ex Münchh. tree. Pectenia plumbea (Lightf.) P.M.Jørg., L. Lindblom, Wedin & S. Ekman, Sticta fuliginosa (Dicks.) Ach., and Teloschistes 1. Albariña, Negreira, A Coruña, Galicia, 200 m, 2301 flavicans (Sw.) Norman were observed in surrounding trees. l/m2, 12.3ºC (Paramos station). This is a small stand of Beba 2, with most of the thalli colonized by the lichenicolous deciduous forest, mainly with Castanea sativa, located fungus Arthonia pelvetii (Hepp. ex Linds.) H.Olivier (Fig. 2a), along Albariña stream and surrounded by Eucalyptus which might affect their survival. One Sambucus tree hosted plantations. Accompanying species were Normandina 20 thalli from the base up to a height of c. 3 m, accompanied pulchella (Borrer) Nyl., Nephroma tangeriense (Maheu by Leucodermia leucomelos, Nephroma tangeriense, and & A.Gillet) Zahlbr., Pannaria conoplea (Ach.) Bory, Pectenia plumbea, whereas another tree had 10 thalli of P. Parmeliella triptophylla (Ach.) Müll.Arg., and Sticta aurata growing together with Nephroma tangeriense and limbata (Sm.) Ach. Other lichen species observed in the Sticta limbata. The thalli growing on a mossy Sambucus trees around were Leucodermia leucomelos (L.) Kalb and nigra tree were not parasitized. Beba 3, with most of the thalli Lobarina scrobiculata (Scop.) Nyl. also infected by Arthonia pelvetii, which may affect the future of this subpopulation. Main accompanying species were 2. Beba, Mazaricos, A Coruña, Galicia. 250 m, 2243 l/ Nephroma laevigatum Ach. and Sticta fuliginosa. Finally, m2, 12.2ºC (Coto Muíño station). This well-preserved forest Beba 4, with accompanying species Lobarina scrobiculata, is located along a tributary stream of Xallas river but is Nephroma laevigatum, and Sticta fuliginosa. threatened because of the surrounding Eucalyptus and Pinus plantations. Main tree species are Castanea sativa, Corylus 3. Devesa de Anllares, Negreira, A Coruña, Galicia, ca. avellana L., Crataegus monogyna Jacq., Quercus robur, and 270 m, 2243 l/m2, 12.2ºC (Coto Muíño station). This is a Sambucus nigra L. Pseudocyphellaria aurata was detected very well-preserved forest along the Xallas river that lacks a in four spots along Beba stream, growing on bark of standing protection figure and is highly threatened due to the surrounding trees and mostly in the south or southeast aspects. Four Eucalyptus plantations and the construction of mini hydropower

Anales del Jardín Botánico de Madrid 77(2): e099 2020. ISSN: 0211–1322. doi: http://dx.doi.org/10.3989/ajbm.2558 Olariaga & al. 4

Fig. 1. Map of the 15 reports of the epiphytic macrolichen Pseudocyphellaria aurata with specific locality in mainland Spain. Type of records: newly discovered (blue), possibly extinct (red), unplausible localities (white). Localities are numbered as in the text.

Fig. 2. Thallii of Pseudocyphellaria aurata in the field: a, Thallus of Pseudocyphellaria aurata showing infection by Arthonia pelvetii in Beba (A Coruña); b, Thallus with an apothecium in Devesa de Anllares (A Coruña). stations. The forest is composed mainly of Castanea sativa, bark of 7 different Quercus robur trees, although one of them Crataegus monogyna, Fraxinus excelsior L., and Quercus was fallen; all the specimens were found on the southern or robur. We detected 31 thalli of Pseudocyphellaria aurata on southwestern aspect. The number of thalli on the trees ranges

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between 1 to 10, and with a size that varies from 0.5 × 0.5 to where we could see at least four thalli on a medium-sized 16 × 18 cm. Most thalli had only soralia but one of them had Alnus glutinosa (L.)Gaertn. almost devoid of other lichens at an apothecium (Fig. 2b). Accompanying species, many of them the base. However, thalli of P. aurata grew at 6–8 m height with euoceanic affinities, were Hypotrachyna sinuosa (Sm.) with other lichens like Hypotrachyna revoluta (Flörke) Hale Hale, Leucodermia leucomelos, Ricasolia amplissima (Scop.) and Lobaria pulmonaria. One of the thalli was large (c. 15 cm De Not. (Dendriscocaulon umhausense (Auersw.) Degel. diam.) and in good shape. This trunk was broken and hanging state), Ricasolia virens (With.) H.H.Blom & Tønsberg, Lobaria by the middle and the thalli of Pseudocyphellaria were then pulmonaria (L.) Hoffm. (abundant with apothecia), Nephroma at 1–2 m high. As this tree was about to fall down, four small tangeriense, Normandina pulchella, Pannaria rubiginosa (Ach.) lobules were translocated to other trees in the vicinity with Bory, Parmeliella triptophylla, Pectenia cyanoloma (Schaer.) similar conditions. Their evolution has not been checked yet. P.M.Jørg., L.Lindblom, Wedin & S.Ekman, P. plumbea, Sticta 6. Intzola erreka, Basque Municipal Community, Pyrenées limbata, Sticta sylvatica (Huds.) Ach., Teloschistes flavicans, atlantiques, France; Bera-Vera de Bidasoa, Navarra. 110– and ferns such as Dryopteris guanchica Gibby & Jermy, and 2 200 m, 1857 l/m , 13.2ºC; obtained from Bera-Larrategaña Hymenophyllum tunbrigense (L.) Sm. station). This population is located c. 1 km E from Ibardin 4. Santa Leocadia, Mazaricos, A Coruña, Galicia. 300 m, pass, along Intzola stream. The upper 1.5 km of Intzola 2243 l/m2, 12.2ºC (Coto Muíño station). This population is stream is in Spain and it crosses the border with France before located along the Vao da Denonciña stream in a deep valley. merging with Urdazuri-Nivelle river several kilometres The riparian forest along the stream harbours euoceanic downstream. Jovet referred (1941) to this site 500 m far ferns such as Hymenophyllum tunbrigense and Woodwardia from the milestones 18 and 19 delimiting the Spanish-French radicans (L.) Sm. The forest is composed mainly of Corylus border as “ravin de Berra”, which is seemingly a misspelling avellana, Crataegus monogyna, Fraxinus excelsior, Laurus of “Bera”. The actual name of the stream running between nobilis L., and Quercus robur. Main accompanying species milestones 18 and 19 is Intzola or Izola (Capdevila i Subirana were: Leucodermia leucomelos, Lobarina scrobiculata, 2009). The zone has large deforested areas intermixed with Nephroma tangeriense, Normandina pulchella, Pannaria forest stands with scattered large pollard oak trees (Quercus rubiginosa, Parmeliella triptophylla, Sticta limbata, and S. robur) and riparious vegetation with Alnus glutinosa, sylvatica. Three subpopulations were found in this locality Fraxinus excelsior, Corylus avellana, and Salix atrocinerea, (Table 1): Santa Leocadia 1, where we found eight thalli on along with scattered planted Platanus hispanica trees. Two six trees, four Corylus avellana and two Laurus nobilis trees, subpopulations were documented (Table 1): Intzola 1, which respectively. Santa Leocadia 2, with two thalli on a Corylus is the site reported by Jovet (1941), located where Intzola avellana tree and two more on a Quercus robur tree. Santa stream and a smaller tributary descending from Ibardin Leocadia 3, with seven thalli on two Q. robur trees, from the merge. We detected P. aurata in two non-pollarded Q. robur base up to a height of c. 4 m in one of the trees. trees, in a rather open and light-exposed location (Fig. 4a-b). One of the trees harboured 10 thalli of P. aurata dispersed 5. Bertiz Natural Park, Bertizarana, Navarra. 200–230 m, 2 from the base up to a height of c. 8 m. Accompanying 1508 l/m , 15.2ºC (Iñarbegi NG station). This protected area mosses and lichens are Coenogonium luteum (Dicks.) Kalb has been poorly managed since the late Middle Age and it & Lücking, Flavoparmelia caperata (L.) Hale, Leptogium constitutes one of the better-preserved old-growth forests in sp., Ricasolia virens, Parmeliella tryptophylla, Parmotrema the northern Iberian Peninsula and southern Europe. Nearly perlatum (Huds.) M. Choisy, Pertusaria pertusa (L.) Tuck., the entire reserve is covered by beech (Fagus sylvatica L.) Pertusaria flavida(DC.) J.R.Laundon, Sticta fuliginosa, and oak (Quercus robur) forest, with an abundant presence Brachythecium sp., Frullania sp., Homalothecium sericeum of pollard-trees and riparious vegetation along its numerous (Hedw.) Schimp., Hypnum cupressiforme Hedw., Neckera streams. We have detected the presence of Pseudocyphellaria complanata (Hedw.) Huebener, and Zygodon viridissimus aurata in two spots along Aranea stream along the track (Dicks.) Brid. A second tree was hollow and burnt towards Plazazelai, 500 m. apart from each other. Two inside. This tree hosted 23 thalli. Accompanying species: subpopulations were found at this locality (Table 1): Bertiz Flavoparmelia caperata, Ricasolia virens, Normandina 1, where we found two thalli (one big and sorediate; the pulchella, Parmotrema crinitum (Ach.) M.Choisy, other one small), found in April 2015 on the bark of Salix Nephroma laevigatum, Pertusaria sp., Brachythecium sp., atrocinerea Brot., with presence of Leptogium brebissonii Metzgeria furcata (L.) Corda, Neckera crispa Hedw., and Mont., Pannaria conoplea, P. rubiginosa and Sticta Zygodon viridissimus (Fig. 5). Jovet (1941) described that fuliginosa, small thalli of Ricasolia virens and abundant thalli of Pseudocyphellaria aurata grew on several oak trees Lobaria pulmonaria and Frullania sp. The Salix tree is (“plusieurs Chênes”). Despite our efforts, 80 years later, P. located near a track and is rather sun-exposed and is rather aurata has only been spotted in two trees indicating that old with numerous dead branches colonized by the polypore the number of colonized trees is probably in decline. The Daedaleopsis tricolor (Bull.) Bondartsev & Singer (Fig. 3). specimen collected by Jovet is deposited in PC (PC 0072622). Two years later (23December 2017) no thalli of P. aurata were found on the same tree, so we suspect that this subpopulation The second subpopulation is Intzola 2, located c. 1.7 km may have gone extinct. The other subpopulation is Bertiz 2, upstream, where two Platanus hispanica trees with large

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Fig. 3. Subpopulation Bertiz 1, Navarra: a, Tree where Pseudocyphellaria aurata was located; b, Same tree from the opposite perspective; c, Sorediate thalli of P. aurata. Arrows indicate the spot where thalli of P. aurata grew. thalli of Lobaria pulmonaria (Fig. 4c-d) stand out. One of 7. Caaveiro, Fragas do Eume Natural Park, A Coruña, these trees hosts c. 64 thalli of Pseudocyphellaria aurata. Galicia. This locality was first reported by Carballal & al. A few more thalli were found on the ground around the tree (1985), based on a specimen collected in 1978 made by an base, attached to detached bark pieces. Accompanying species unknown collector (SANT-Lich 133). Population size was not were: Lobaria pulmonaria, Ricasolia virens, Nephroma reported. Pseudocyphellaria aurata has not been observed laevigatum, Brachythecium sp., Eurhynchium praelongum again at this site, although the locality has been often visited (Hedw.) Schimp., Metzgeria furcata, Isothecium myosuroides (López de Silanes, pers. comm.). Fragas do Eume Natural Brid., and Neckera complanata (Hedw.) Huebener. Park is a well preserved and protected coastal deciduous forest, where habitat loss or degradation should not have Previous localities caused decline or extinction of P. aurata during the past 40 years. Nevertheless, the lack of recent observations suggests Burgaz & Martínez (1999, 2003) reported that population size of P. aurata is very small, or even, that Pseudocyphellaria aurata only from A Coruña in Spain and the species might have become extinct. from three provinces in Portugal. However, P. aurata has been cited from more localities, and other specimens from 8. Bayona, Pontevedra, Galicia. A correctly identified Spain exist also in herbaria. Detail examination all these specimen of Pseudocyphellaria aurata collected by Lázaro previous reports is of paramount importance to assess a Ibiza is kept at the MAF herbarium (MAF-Lich 12139), but possible decline of P. aurata in the Iberian Peninsula, and for to our knowledge, this locality was never reported in his the application of the criteria of the IUCN. Thus, we provide publications. Although there are no recent reports of P. aurata below a commented list of 11 previous reports of P. aurata from Pontevedra, we consider the presence of P. aurata there in mainland Spain, listed from most recent to oldest. Most of very likely in the past due to suitable climatic conditions. This these records were not included in Burgaz & Martínez (1999, population, however, is likely to have disappeared as a result 2003). Localities are also represented on a map (Fig. 1). of habitat degradation.

Anales del Jardín Botánico de Madrid 77(2): e099 2020. ISSN: 0211–1322. doi: http://dx.doi.org/10.3989/ajbm.2558 7 Rediscovery of Pseudocyphellaria aurata in Spain

Fig. 4. Population Intzola, Navarra: a, Trees where Pseudocyphellaria aurata was located in Intzola 1 subpopulation; b, Thalli of P. aurata growing together with Ricasolia virens in subpopulation Intzola 1; c, Tree where P. aurata grew in subpopulation Intzola 2; d, Same tree from another perspective; d, Close-up showing thalli of P. aurata growing on loose bark of Platanus hispanica. Arrows indicate trees on which thalli of P. aurata grew.

9. Lekeitio (Biscay). Jovet (1941), apparently after a presence of P. aurata in this locality feasible in the past, but it communication by P. Allorge, indicated that Pseudocyphellaria appears to have gone extinct due to habitat loss and degradation. aurata was found “sur des Quercus dans des ravins maritimes accidentés à 25 m. de la mer, 1933”. Regrettably, no herbarium 10. Moncayo (Zaragoza, La Rioja or Soria). This location specimen supports this finding. This is a botanically remarkable was first cited by Colmeiro (1889) indicating “Láz.” (Blas locality because of the presence of rich stands of Woodwardia Lázaro e Ibiza) as the collector, and was later mentioned by radicans and Stegnogramma pozoi (Lag.) K.Iwats. (Allorge Lázaro e Ibiza (1898) and Longinós Navás (1903, 1908). & Allorge 1941), which are associated to warm hyperoceanic Interestingly, a specimen labelled as collected in Moncayo, climates. Etayo (2009) visited this locality and could not find without date, is kept in the Lázaro e Ibiza herbarium (MAF- P. aurata there. Recently, we visited all the ravines that had Lich 12135). The presence of P. aurata in Moncayo is unlikely forest in 1945 (Egurbideko erreka, Portuko erreka, Burgañeko since the continental climate with cold winters is unsuitable for erreka) covering the area between Lekeitio and Ondarroa, P. aurata and for other more common species of the Lobarion where P. Allorge and V. Allorge have made collections. At alliance. However, this specimen represents beyond doubt P. present, those ravines present patches of rather degraded forest aurata. Pseudocyphellaria aurata has not been observed in with few mature oak trees, where we could not find P. aurata Moncayo again and we thus propose that the locality given in or any species of the Lobarion communities. We consider the the label is incorrect.

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11. Monasterio de Piedra (Zaragoza). A specimen 16. Without locality. Colmeiro (1867) listed Lagasca collected by Lázaro e Ibiza in 1894 is kept in the MAF as the collector of this specimen of Pseudocyphellaria herbarium (MAF-Lich 111914). Lázaro e Ibiza omitted aurata. Nevertheless, this report seems to correspond to this locality in his account of Spanish lichens in 1898. Pseudocyphellaria crocata, as Colmeiro merged P. aurata The specimen cited above represents P. aurata beyond and P. crocata into a single species. We have checked the doubt, but no later observation of this species could be Spanish specimen sent by Lagasca and seen by Acharius traced in Monasterio de Piedra. As in the previous case, the (1810), identified as P. crocata (H-Ach without number). No presence of P. aurata in this continental locality is difficult other collection of P. crocata has been made in Spain ever to conceive and we propose that the label locality of the since and this suggests, if the country information is correct specimen is incorrect. and the specimen of P. crocata was indeed collected in Spain, 12. Villarluengo (Teruel). This locality was mentioned it is very possible to have become extinct in continental Spain. by Colmeiro (1867) citing “Xarne” (Agustín Xarne) as the An alternative is that the Spanish specimen was collected in collector. This information might have been obtained from the Canary Islands, where P. crocata is not rare, but Lagasca an unpublished list of plants by Xarne (“Plantas observadas is not known to have travelled there. en este término de la villa de Villarluengo”), but there are 17. Without locality. Fries (1831) listed P. aurata from not specimens supporting it. We regard this record as very Spain based on a specimen collected by L. Dufour, who doubtful due to the oceanic requirements of P. aurata and we travelled to Spain in 1826 (Fries 1831). However, no specimen propose that it might be a misidentification. supporting this report could be traced in the Fries herbarium 13. Algeciras, Cádiz. This record corresponds to a (UPS-Fries). herbarium specimen collected by Bourgeau, without date, deposited in PC (PC 0072591). This specimen was probably DISCUSSION collected in 1849 or 1853 when E. Bourgeau (1815–1877) Examination of bibliographic and herbarium data yielded visited Andalusia (Carrasco & al. 2002) and was later new and noteworthy information on Pseudocyphellaria included by Jovet (1941) in his locality list. The specimen aurata in peninsular Spain. In addition, six new localities were represents undoubtedly P. aurata, and is the only one discovered after a focused search in suitable habitats and this known from southern mainland Spain. Pseudocyphellaria suggests that more not-yet-discovered localities might exist. aurata is probably extinct in this area. The species has not In one of them, a thallus with a single apothecium was found, been detected in Andalusia (Burgaz 2014) since Bourgeau’s which represents, as far as we know, the first fertile specimen record, despite several lichen field surveys conducted in the ever observed in Europe. On the other hand, the existence of Algeciras area. a number of herbarium specimens and bibliographic reports 14. Alcalá de los Gazules and Ubrique (Cádiz), Sauceda during the 19th century suggest that P. aurata was considerably de Cortes (Málaga). These three localities were also listed by more widespread in Spain in the past. Colmeiro (1867) citing “Clem.” (Simón de Rojas Clemente) This study confirms that Pseudocyphellaria aurata is as collector. These localities were probably obtained by not extinct in mainland Spain, where it had not been seen Colmeiro through an unpublished manuscripts by Clemente, since 1978, nor has it become extinct in the Pyrenees. or from private correspondence. Degelius (1935) also Considering that P. aurata is an eye-catching, easily included these localities in his distribution map of P. aurata. recognizable macrolichen, the number of new localities found Regrettably, most part of the Clemente herbarium is lost is remarkable. All newly discovered localities constitute (González Bueno & Rico 1991) and specimens from these well-preserved patches of Atlantic forest along streams, in localities are not available. Two of us visited Alcalá de los areas with strong oceanic influence and mild winters. Forests Gazules and Sauceda de Cortes in March 2018, and although where P. aurata was found have had ecological continuity well-preserved Lobarion communities were observed in but have been exploited in the past as suggested by the Sauceda de Cortes, P. aurata could not be found. As we have presence of pollarded trees. The presence of P. aurata on a seen material of P. aurata from Algeciras, we consider these planted Platanus hispanica suggests that P. aurata is also reports are likely to be correct. Although P. aurata might be able to grow in somewhat disturbed forest patches. Atlantic extinct in the area, it should be searched for again in these deciduous forests, the exclusive habitat of extant populations localities. of P. aurata in Spain, have undergone a strong decline due to 15. Salamanca area. This area was marked by Degelius human pressure, forestry and crop establishment (Blanco & (Fig. 43, 1935) with an empty point on the map of al. 1998) and P. aurata has probably declined likewise. Forest Pseudocyphellaria aurata. According to our search, empty patches were P. aurata is now found are in general small, points refer to reports without a specific location and we thus fragmentary, and harbour small populations of P. aurata, with suspect the source of Degelius was Lázaro e Ibiza (1920), few trees colonized and few individuals. Except for the Bertiz who mentioned P. aurata in “C., S. y O.” of Spain. Although, population, a large (2040 ha) nature reserve of remarkably Jovet (1941) also mentioned this locality, we think it is likely well-preserved deciduous forest, forestry is an important erroneous. threat for known populations of P. aurata. Extant populations

Anales del Jardín Botánico de Madrid 77(2): e099 2020. ISSN: 0211–1322. doi: http://dx.doi.org/10.3989/ajbm.2558 9 Rediscovery of Pseudocyphellaria aurata in Spain of P. aurata have, as small populations usually do, a higher present status of P. aurata at a European scale and following risk of extinction. Dynamics of populations of P. aurata are the criteria of the International Union for Conservation of difficult to assess due to lack of data, but the number of trees Nature (IUCN), for which the present account of Spanish colonized by P. aurata seems to have decreased in Intzola 1 populations will be helpful. subpopulation; Jovet (1941) saw P. aurata in several oak trees but it is currently present only in two. ACKNOWLEDGEMENTS The critical analysis of previous records found in We wish to thank José Pizarro (MAF) and Leena Myllys (H) for the literature and herbarium specimens suggests that the kindly sending us scans of historical material or specimens on loan. distribution area of Pseudocyphellaria aurata has been reduced and that local extinctions have occurred. The REFERENCES species is distributed in areas of temperate oceanic climate Acharius E. 1810. Lichenographia universalis. Gottingen, Germany. and mild winters in Europe (Sérusiaux 1989). Thus, reports Allorge V. & Allorge P. 1941. Les ravins à Fougères de la corniche vasco- from Lekeitio (Biscay) and Bayona (Pontevedra), this last cantabrique. Bulletin de la Société Botanique de France 88: 92–111. 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